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157
Focal High Signal on MR Scans of the Midbrain Caused by Enlarged Perivascular Spaces: MR-Pathologic Correlation
Dan
Allen D. Elster1 N. Richardson
Punctate in the
foci of abnormal
and linear
midbrains
of 32 (20%)
of 157
signal
patients
were
observed
undergoing
near the substantia
high-resolution
MR
nigra
imaging
of
the brainstem. The lesions were most easily seen on bong TR/Iong TE images, where they were of high signal intensity. Their location was consistently in the bower mesencephalon near the junction of the substantia nigra and cerebral peduncle. Unilateral lesions were observed in 18 cases, while bilateral lesions were noted in 14. A review of anatomic specimens revealed the constant presence of penetrating branches of the coblicular or accessory cobbicubar arteries in this location. Enlarged perivascular spaces around these vessels were frequently seen in the specimens and probably account for punctate and linear foci observed on high-resolution MR images of the
midbrain.
AJNR
I 1:1 1 19-1
122,
November/December
1990;
AJR
156:157-160,
January
1991
Punctate foci of high signal on T2-weighted images of the brain have long excited curiosity and interest. Initially dubbed “UBOs,” on “unidentified bright objects,” the anatomic and pathologic correlates of these lesions are gradually being explained. Known causes of these lesions include enlarged penivascular spaces, atrophic penivascular demyebination, white matter infarctions, capillary tebangiectasias, congenital brain cysts, ventricular diverticula, ependymitis granulanis, and isomorphic gliosis [1 -9]. When no particular causative factor is identified, the descriptive term “beuko-araiosis” has been applied to these lesions [10]. Although these lesions were initially observed supratentonially, several investigators have noted that similar-appearing lesions may also be found in the brainstem [1 , 6]. These brainstem lesions are relatively common in elderly patients, are located predominantly in the pons, and frequently possess ill-defined margins. Recently, we began to observe a different type of brainstem lesion in several young patients undergoing high-resolution MR imaging of the posterior fossa. These lesions were punctate and linear foci typically located near the substantia nigna and cerebral peduncle in the lower mesencephabon (Fig. 1). Because of their consistent location and shape, we speculated that these midbrain lesions represented anatomic structures rather than being merely nonspecific white matter abnormalities. We therefore set out to investigate systematically the frequency of these lesions and to establish their true identity. Received May 3, 1990; revision requested June 4, 1990; revision received June 18, 1990; accepted July 2, 1990. 1 Both authors: Department of Radiology, Bowman Gray School of Medicine, Wake Forest University, 300 5. Hawthorne Ad. , Winston-Salem, NC 27103. Address reprint requests to A. D. Elster.
0361-803X/91/1561-0157 C American
Roentgen
Ray Society
Materials During
and
Methods
an 1 8-month
period,
1 57 patients
were
referred
to us for high-resolution
MR
studies
of the cerebellopontine angle and temporal bone. The patients ranged in age from 28 to 82 years old (median, 45 years). Approximately 90% (1 41/1 57) of these patients were referred from our otolaryngology service for hearing loss or vertigo, with the principal clinical injunction to “rule out acoustic neurinoma.” The remaining patients were referred for a variety of lesions involving the temporal bone, including postoperative complications, infections, and neoplasms.
158
ELSTER
AND
RICHARDSON
AJR:156,
January 1991
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Fig. 1.-Punctate and linear foci (arrows D) of abnormal signal seen in midbrain. A, Axial TI-weighted image (600/20/2). sion on left has a more linear configuration. B, Coronal Ti-weighted image (600/20/2). C and D, Axial and coronal T2-weighted ages (2000/120/2).
in ALe-
im-
No patient in this series had symptoms or signs referable to the midbrain, as determined by review of a three-page medical questionnaire completed by each patient prior to imaging. All scans were acquired at 1 .5 T (Picker Vista MA, Highland Heights, OH). The scans analyzed were from a triple-echo protocol with parameters of 2000/40, 80, 1 20/2 (TA/TEs/excitations). Slices were 3.5-mm thick with a 0.5-mm gap, and the images analyzed were
collection, the ages and clinical status of the donors being unknown. All brains were fixed in formalin, then embedded in paraffin, sectioned at 40 m, and stained with H and E. The sections were viewed with low-power light microscopy using magnification of up to x200. Aeference to a major brainstem anatomy text was made in order to assign specific identities to the structures visualized [11].
exclusively
Results
from
the
coronal
plane.
Other
scan
parameters
included
a field of view of 20 cm and an image
acquisition matrix of 192 x 256. Axial T2- and Ti-weighted images were inconsistently obtained through the upper midbrain, so these were not used in the statistical tabulation. Where available and appropriate, however, images from these sequences were retained for purposes of illustration. Similarly, since all patients were referred for suspected disease involving primanly the cerebellopontine angles or temporal bone, complete images of the rest of the brain were obtained only occasionally in fewer than 1 5 patients. The MA scans were retrospectively reviewed by the authors to determine
the frequency
of punctate
and
linear
foci
seen
in the
lateral
and inferior mesencephalon as illustrated in Figure 1 . High-signal foci were scored by consensus of the readers as either present or absent in each case. If present, the lesions were further scored as being present unilaterally or bilaterally. Following the retrospective analysis of the MA scans, we reviewed serial midbrain sections from 25 cadaver brains. These specimens were selected at random from a medical school anatomy laboratory
Punctate and linear images were identified patients. In 1 8 cases
foci of high signal on T2-weighted MR in the midbrains of 32 (20.4%) of 157 the lesions were unilateral and in 14
cases they were bilateral. The lesions were consistently 10cated in the lower mesencephabon near the substantia nigra, cerebral peduncbe, and decussation of the brachium conjunctivum. Representative examples are shown in Figure 1. The lesions seen were approximately 1 -1 .5-mm in greatest dimension and were frequently more ovoid or linear than round. They were best seen on the TE 1 20 images, and (when performed) also on the Ti -weighted images. On all pulse sequences used they maintained isointensity with CSF. Since our study was not prospectively designed and since complete images of the rest of the brain were not routinely obtained, we did not attempt to correlate the presence of these midbrain lesions with supratentorial white matter lesions
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AJA:156,
January 1991
ENLARGED
MIDBRAIN
PERIVASCULAR
or enlarged penivascular spaces elsewhere in the brain. We found no significant differences in the ages of the patients with midbrain lesions (28-79 years) and those without such lesions (29-82 years). Since nearly all patients in both groups were referred for suspicion of acoustic neurinoma, there were likewise no significant differences between the two groups with regard to clinical symptomatobogy. Enlarged perivascular spaces near the anterior commissure were seen in association with the midbrain lesions in several patients who had complete brain studies; conversely, several patients had midbrain lesions as an isolated finding. Review of the anatomic specimens revealed the constant (25/25 cases) presence of small, penetrating vessels in the infenolaterab midbrain (Fig. 2). The vessels seen were identified
as branches
of the cobliculan and accessary
collicubar arteries,
which are themselves branches of the posterior cerebral artery. In six of these specimens, prominent perivascubar spaces measuring larger than i mm in greatest dimension were observed. These penivascubar spaces were of the appnopniate size, location, and orientation such that they could reasonably account for the punctate and linear foci of high signal seen on MR images of the midbrain.
literature reveals that the enlarged perivascubar spaces in the midbrain we have observed most likely surround penetrating branches of the collicubar and accessory cobbiculan arteries (Fig. 3). The crus
plied primarily
cenebri
and anterolaterab
midbrain
by rami of these arteries.
are sup-
The collicular
artery
is a small but constant vessel that arises from the posterior cerebral artery in the interpeduncular fossa [1 1 ]. Here the artery lies in close relation to radicles of the ocubomotor nerve.
Exiting the interpedunculan fossa the collicubar artery first traverses the anterior surface of the crus cerebri, closely following the pontomesencephalic sulcus. Upon reaching the lateral margins of the crus, the colbiculan artery ascends across its lateral side reaching the lateral mesencephalic sulcus. Thereafter, the artery inclines sharply posteriorly to reach the brachium of the inferior colbiculus. Here it divides into its two terminal branches that supply the superior and inferior colliculi, respectively. In most specimens an accessory collicular artery may also
be found. This vessel branches from the proximal segment of the main cobbiculan artery, following it closely upon its upper side as far as the lateral mesencephabic subcus. Both the main and accessory collicular arteries give rise to numerous penetrating branches that supply the cerebral peduncle, substantia nigra, and lateral portion of the red nucleus. These arteries
Discussion
have a steeply
Over the last 2 years, several investigators
have noted that
enlarged penivasculan spaces are responsible for producing punctate lesions on MR scans in the brains of otherwise healthy individuals [1 , 2, 7-9]. These enlarged perivascubar (Virchow-Robin) spaces are commonly seen in two locations: along the anterior commissure into the bower basal ganglia and at the brain vertex. The MR signal characteristics of these penivascular spaces are such that they maintain isointensity with CSF on all pulse sequences used. The midbrain lesions
we observed
have MR signal characteristics
tent with that the brain.
reported
Review
159
SPACES
of serial
for penivascubar
anatomic
specimens
entirely
spaces
consis-
elsewhere
and the anatomic
in
counting ages.
Each
oblique
for their
course
segmental
penetrating
through
the brainstem,
visualization
mesencephalic
on serial
artery
ac-
MR
is often
im-
closely
accompanied by a satellite vein. Frequently, several veins and arteries are seen grouped into a small pedicle for some distance after penetrating the lateral margin of the crus cerebri. The penetrating veins drain outward to the lateral mes-
encephalic vein. This vessel in turn links the basal vein to the superior petrosal vein. We were unable to observe any venous structures surrounding specimens. signalfrom
of size comparable to the penivascular spaces the colliculan arteries in any of our anatomic It remains possible, however, that in some cases slowly flowing blood in the satellite veins described
.
,
-..
.
.
%P
.*..,
.
‘I
::. :.
\“ -j:.;..
Fig. 2.-Anatomic
specimens
-,,.
.
(H and E stain)
of midbrain (m) and pons (p). A, Coronal section (x5). Enlarged perivascular spaces surrounding collicular artery are seen on left (double arrows). A normally sized perivascular space is noted on right (single arrow). B, Higher power view of A (x50). Branches of collicular artery (a) are seen surrounded by enlarged Virchow-Robin space The perivascular space is lined by pia (arrowheads). Note pigmented cells of substantia nigra nearby (arrows).
. .
B
I. ‘
:
.,
.
:
‘.
‘:
160
ELSTER
AND
RICHARDSON
AJA:156,
January
1991
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should not be mistaken for lacunar infarcts on nonspecific white matter changes when seen in this characteristic location.
Usual location of enlarged perivascularspaces
REFERENCES 1 . Braffman
BH, Zimmerman
Periventricular
Fig. 3.-Diagram of blood supply to lateral midbrain. Penetrating branches of collicular artery (CA) and accessory collicular arteries (ACA) routinely supply the region where enlarged penvascular spaces are found. CP = cerebral peduncle, SN = substantia nigra, ML = medial lemniscus, SCP = decussation of superior cerebellar peduncle, IC = inferior colliculus, PAG = periaqueductal gray matter.
above may contribute to the linear and punctate midbrain lesions we have described. In conclusion, we believe that small foci of high signal seen in the inferior and lateral midbrain represent enlarged penivascular spaces associated with penetrating branches of the collicular and accessory collicular arteries. Such lesions
RA, Trojanowski
JQ, et al. Brain MA: pathologic
with gross and histopathology. 1 . Lacunar infarction and Virspaces. AJNR 1988;9:621-628 2. Braffman BH, Zimmerman AA, Trojanowski JO, et al. Brain MA: pathologic correlation with gross and histopathology. 2. Hyperintense white-matter foci in the elderly. AJNR 1988;9:629-636 3. Kirkpatrick JB, Hayman LA. White matter lesions in magnetic resonance imaging of clinically healthy brains of elderly subjects: possible pathologic basis. Radiology 1987; 162:509-511 4. Zimmerman AD, Fleming CA, Lee BCP, Saint-Louis LA, Deck MDF. correlation chow-Robin
hyperintensity
as seen by magnetic
resonance:
prevalence
and significance. AJNR 1986;7: 13-20 5. Sze G, DeArmond SJ, Brant-Zawadski M, et al. Foci of MAI signal (pseudo lesions) anterior to the frontal horns: histologic correlations of a normal finding. AJNR 1986;7:381-387 6. Salomon A, Yeates AE, Burger PC, Heinz EA. Subcortical arteriosclerotic encephalopathy: 1987;165:625-629
brain
stem
findings
with
MA
imaging.
Radiology
7. Jungreis CA, Kanal E, Hirsch WL, et al. Normal perivascular spaces mimicking lacunar infarction: MA imaging. Radiology 1988;1 69:101-104 8. Drayer BA. Imaging of the aging brain. I. Normal findings. Radiology 188;166:785-796
9. Heier LA, Bauer C, Schwartz L. Zimmerman AD, Deck MDF. Large Virchow-Aobin spaces: MA-clinical correlation (abstr). AJNR 1988;9 :1033. 10. Hachinski VC, Potter P. Merskey H. Leuko-aralosis. Arch Neurol 1987;44:21-24 HM. 1978:16-66
1 1 . Duvernoy
Human
brainstem
vessels.
Berm:
Springer-Verlag,